Human infections associated with wild birds

Journal of Infection (2008) 56, 83e98

www.elsevierhealth.com/journals/jinf

REVIEW

Human infections associated with wild birds

Sotirios Tsiodras a,*,g, Theodoros Kelesidis b,g, Iosif Kelesidis b,Ulf Bauchinger c,f, Matthew E. Falagas d,e

a University of Athens Medical School, 1 Rimini Street, Xaidari, 12462 Athens, Greeceb Beth Israel Deaconess Medical Center, Harvard University Medical School, Boston, MA, USAc University of Munich (LMU), Planegg-Martinsried, Germanyd Alfa Institute of Biomedical Sciences, Athens, Greecee Department of Medicine, Tufts University School of Medicine, Boston, MA, USAf Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev, Ben-Gurion, Israel

Accepted 1 November 2007Available online 21 December 2007

KEYWORDSCommunicablediseases;Avian infection;Wild birds;Infectious diseases;Influenza;Lyme disease;Arbovirus;West Nile encephalitis;Enteric infection;Antimicrobialresistance

* Corresponding author. Tel.: þ30 21E-mail address: [email protected]

g The first two authors contributed e

0163-4453/$30 ª 2007 The British Infedoi:10.1016/j.jinf.2007.11.001

Summary Introduction: Wild birds and especially migratory species can become long-distancevectors for a wide range of microorganisms. The objective of the current paper is to summarizeavailable literature on pathogens causing human disease that have been associated with wildbird species.Methods: A systematic literature search was performed to identify specific pathogens known tobe associated with wild and migratory birds. The evidence for direct transmission of an avianborne pathogen to a human was assessed. Transmission to humans was classified as direct if thereis published evidence for such transmission from the avian species to a person or indirect if thetransmission requires a vector other than the avian species.Results: Several wild and migratory birds serve as reservoirs and/or mechanical vectors (simplycarrying a pathogen or dispersing infected arthropod vectors) for numerous infectious agents. Anassociation with transmission from birds to humans was identified for 10 pathogens. Wild birdsincluding migratory species may play a significant role in the epidemiology of influenza A virus,arboviruses such as West Nile virus and enteric bacterial pathogens. Nevertheless only one caseof direct transmission from wild birds to humans was found.Conclusion: The available evidence suggests wild birds play a limited role in human infectiousdiseases. Direct transmission of an infectious agent from wild birds to humans is rarely identified.Potential factors and mechanisms involved in the transmission of infectious agents from birds tohumans need further elucidation.ª 2007 The British Infection Society. Published by Elsevier Ltd. All rights reserved.

0 5831989, þ30 6932 665820; fax: þ30 210 5326446..gr (S. Tsiodras).qually to this work.

ction Society. Published by Elsevier Ltd. All rights reserved.

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84 S. Tsiodras et al.

Introduction

Free-living birds, including migratory species, can becomelong-distance vectors for a wide range of microorganismsthat can be transmissible to humans.1 This creates thepotential for establishment of novel foci of emerging orre-emerging communicable diseases along bird migrationroutes.2 Certain pathogens are more often isolated in mi-gratory birds in comparison to other animal species3,4 andthe potential for transport and dissemination of thesepathogens by wild birds is of increasing public health con-cern stimulated by the recent spread of diseases likehighly pathogenic Avian influenza A (HPAI H5N1 Asianlineage) and West Nile virus (WNV) infection.3,5 Avianinfluenza A (HPAI H5N1 Asian lineage) and West Nile virusinfection, well known to affect birds for decades, havebeen recently observed to affect areas far away fromthe locations where they were originally identified, gener-ating the hypothesis that migratory birds transportedthese pathogens to new geographical locations.6 Howeveras is the case with the highly pathogenic avian influenza,scientific data do not always support such hypotheses.7

Several factors affecting wild bird species including migra-tory species such as increasing stress levels and crowdingpotentially promote infectious disease transmission amongbirds but available data supporting this are scarce or non-existent.

The objective of this paper is to summarize availableliterature on pathogens causing human disease that havebeen associated with wild birds including wild migratorybird species. Although wild bird borne infections can occurat any spatial scale, from very localized, to short and longdistance, from an epidemiologic point of view the trans-mission of pathogens from wild birds to humans over a longdistance is most important. Therefore, in the currentmanuscript we focused more on the role of wild migratorybirds in the spread of certain pathogens. The paperfocuses on available evidence of transmission of avianborne pathogens to humans. We speculated that suchevidence would originate from enhanced animal andhuman surveillance and the application of advancedmolecular diagnostic testing during the recent years.Furthermore, we attempted to identify factors potentiallycontributing to such transmission from the available bodyof science.

Methods

Two reviewers (TK and IK) independently performed theliterature search. The following terms were used insearches of the PubMed database: ‘‘wild birds’’, ‘‘migra-tory birds’’, ‘‘infection’’, and specific pathogens known tobe associated with wild and migratory birds e.g. ‘‘WestNile virus’’, ‘‘avian influenza’’, ‘‘influenza A’’, ‘‘Lyme dis-ease’’ and ‘‘arbovirus’’. We also screened articles relatedto the initially identified publications to expand our datasources. Despite the availability of scientific data on thisissue even before 19668,9 we focused in the modern areawhere molecular diagnostics might enhance our ability tostudy such interactions between birds and humans. Similarsearches were conducted for each individual migratory

bird species identified through a list provided by theRoyal Ornithological Society of Great Britain and Worldbird databases (Avibase World List).10,11 We also used thewidely used Sibley and Monroe Classification for birds.12,13

To evaluate the role of recent diagnostic developments,we also performed an additional search of the literatureby using the term polymerase chain reaction (PCR) and‘‘migratory birds’’. Additional epidemiologic informationfor the identified pathogens-diseases was obtained fromthe websites of the United States Centers for Disease Con-trol (CDC), World Health Organization (WHO), FAO, andOIE.14,15

Study selection and data extraction

The role of wild and migratory birds in the transmission ofan infectious disease to humans was discussed in consensusmeetings where all authors participated. Transmission tohumans was classified as direct if there was evidence fordirect transmission of the pathogen from the avian speciesto humans through direct contact with an infected bird andgenetic/serological evidence of the presence of a particularpathogen in both the avian species and humans. Transmis-sion to humans was classified as indirect if there wasevidence for transmission of the pathogen from the avianspecies to humans through indirect contact with an in-fected bird and genetic/serological evidence of the pres-ence of the particular pathogen in both the avian speciesand humans. We considered indirect ways of transmission,those through contaminated water from feces of water-fowls and through vectors that are carried by wild birdssuch as mosquitoes and ticks (Table 1). Finally, we classi-fied pathogens to be associated with a ‘‘theoretical riskfor transmission’’ when in the literature there were re-ports that these pathogens were isolated both from humansand wild birds, using microbiological, genetic or serologicalmethods, but there were no reports of actual direct/indi-rect transmission of these pathogens from wild birds tohumans. Despite the lack of actual evidence in such cases,the risk exists in theory e.g. through ingestion of watercontaminated from feces of wild birds or exposure toinanimate surfaces contaminated by bird secretions ordroppings.

Compiled relevant bird species data (with formal avianfamily names) are presented in the appendix. This appendixfurther includes data on pathogens that are borne by wildavian species that have not yet been associated with humaninfection in published reports.

Results

Evidence for direct transmission

The systematic review of the literature review identified noreal evidence for direct wild bird to human transmissionwith the only exception being the cluster of H5N1 humancases in Azerbaijan where the affected patients wereplucking feathers from mute swans that had succumbedto H5N1 infection.16

Table 1 Pathogens that have been reported to be indirectly transmitted from wild birds including migratory species to humans

Microorganism(s) Reported transmission to human(indirect transmission) (n Z 10)

Migratory bird species (formal familynames for each bird species can befound in the appendix)

Geographicarea

(I) BacteriaChlamydiaceaeChlamydophila

psittaciOrnithosis17e22 Egrets (Ardea Alba), grackles

(Quiscalus), gulls (Larus), migratorywaterfowl species (Anatidae),passerines (Passeriformes), pigeons(Columbidae), psittacine birds(Psittaciformes), raptors (NorthAmerican raptors), shorebirds (NorthAmerican shorebirds), wild ducks(Anatidae), and others

Worldwide

EnterobacteriaceaeEscherichia coli Bloody diarrhea [Vero cytotoxin-

producing E. coli O157, Shiga toxin stx2f-containing E. coli O128 strain)23,24]25,26

Finches (Fringillidae), gulls (Larus),pigeons (Columbidae), sparrows(Passeridae), starlings (Sturnidae)

Worldwide

Salmonella(entericatyphimurium)

Salmonellosis (enteritis)27e30 Wild crows (Corvidae), ducks(Anatidae), gulls (Larus), passerines(Passeriformes), raptorial birds (NorthAmerican raptors), songbirds(Passeriformes), terns (Sternidae),waterfowls (Anatidae)

Worldwide

MycobacteriaceaeMycobacterium

(avium,ulcerans)

Regarding M. avium it is generallybelieved and occasionally reported thatman (especially immunocompromised,elderly) can contract the disease frombirds, but this has not been fullyclarified.31e33

Crows (Corvidae), raptors (NorthAmerican raptors), rooks (Corvusfrugilegus), wild ducks (Anatidae),wild pigeons (Columbidae)

Worldwide

Possible transmission of M. ulcerans tohumans through contaminated waterfrom feces of waterfowls (Anatidae)34

Spirochaetaceae Lyme disease30,35e41

Borreliaburgdorferisensu latogenomic species

American Robins (Turdus migratorius),cardinals, songbirds (Passeriformes),sparrows (Passeridae), thrushes(Turdidae) and other ground foragingbirds, waterfowl (Anatidae)

North America,Europe

(II) FungiCryptococcus Yes (wild pigeons)42e46 Psittacine birds (Psittaciformes),

starling (Sturnidae), wild pigeons(Columbidae)

Europe, SouthAmerica, Asia

(III) VirusesFlaviviridaeWest Nile virus Yes3,30,47e49 North American shorebirds, common

grackles (Quiscalus quiscula), doves,hawks, house finches (Carpodacusmexicanus), and house sparrows(Passer domesticus), songbirds(Passeriformes), raptors (NorthAmerican raptors), owls (Strigidae),and various corvids (crows, jays,Corvidae)

Africa Europe,Asia, America

(continued on next page)

Wild birds and human infections 85

Table 1 (continued)

Microorganism(s) Reported transmission to human(indirect transmission) (n Z 10)

Migratory bird species (formal familynames for each bird species can befound in the appendix)

Geographicarea

St. Louisencephalitisvirus (SLEV)

Yes3,49e51 North American shorebirds, commongrackles (Quiscalus), doves, hawks,house finches (Carpodacus mexicanus),and house sparrows (Passerdomesticus), songbirds(Passeriformes), owls (Strigidae), andvarious corvids (crows, jays, magpies)

America

Western EquineEncephalitisvirus (WEEV)

Yes49 North American shorebirds, quails(Coturnix)

America

OrthomyxoviridaeInfluenza A virus To date, only domestic poultry are

known to have played a major role in thetransmission cycle of the H5N1 virus fromanimals to humans.52 However, there isalso the potential contribution of otherhosts like carnivores e.g cats to bothvirus transmission and adaptation tomammals.53,54 Dead or moribund catswere found to be infected with H5N1virus soon after the virus was detected inwild birds in Germany.53 This suggeststhat H5N1 virus can be transmitted fromwild birds to cats53 whereas in anotherreport avian influenza A virus subtypeH5N1 was transmitted to domestic catsby close contact with infected birds.54

Dabbling ducks (e.g common Mallard-Anas platyrhynchos), geese(Anserinae), gulls (Larus), swans(Cygninae), guillemots (Uria aalge),mountain hawk eagles (Spizaetusnipalensis) North American Blue-winged Teal (Spatula discors),shearwaters (Procellariidae), terns(Sternidae). Wild aquatic birds areregarded as the principal reservoir ofinfluenza viruses, and migrating ducks(Anatidae) disseminate influenzaviruses worldwide

Worldwide

However, there has been no documentedcase with wild migratory bird to humantransmission although the theoreticalrisk exists.55

Serologic evidence of avian influenzainfection in 1 duck hunter and 2 wildlifeprofessionals with extensive histories ofwild waterfowl (Anatidae) and game birdexposure has been reported.56

There is an association (not necessarilycausal) between recreational contactwith H5N1 contaminated water and theonset of confirmed human H5N1 diseasein 3 cases.53,57,58 In one of these casesasymptomatic ducks may have shed virusinto the pond.53

Possible direct transmission of highlypathogenic avian influenza in familycluster in Azerbaijan.16 Occupationalexposure to avian species may increaseveterinarians’ risk of avian influenzavirus infection.59

Transmission can cause: Respiratoryinfection, keratoconjuctivitis, diarrhea,encephalitis30,60e66



Evidence for indirect transmission or a theoreticalrisk for transmission

Although a large number of avian borne pathogens havebeen identified in the literature, we found relatively scarceevidence for indirect transmission of avian borne pathogensto humans (Table 1). Unfortunately, in the vast majority ofthe reports reviewed herein, data were unavailable to fur-ther characterize the way of transmission of certain patho-gens beyond the stage of a speculative argument. Thiswould be expected for zoonoses which usually require am-plification in an animal species cycle before spill-over tohumans. Nevertheless and based on our criteria severalavian borne bacterial, fungal, viral pathogens could be indi-rectly transmitted or associated with a theoretical risk fortransmission to humans (Table 1). We identified 58 suchpathogens for which wild birds can serve as reservoirs, me-chanical vectors, or both (Tables 1 and 2). However, thepaucity of available data did not allow us to make the dis-tinction whether the involved species serve as reservoir orvector in most of the cases.

Scarce microbiological, serological and epidemiologicaldata supported indirect transmission from wild birds tohuman for 10 of these pathogens (Table 1). Application ofadvanced molecular diagnostic testing during the recentyears has led to the isolation of these microbial agentsknown to affect humans in birds. The examples include bac-terial spp. like Escherichia coli,24,25 Borrelia Burgdorferi,37

Anaplasma phagocytophilum,87 Salmonella typhimurium,28

Campylobacter spp.,79 and Mycobacterium spp.,31e33 vi-ruses like Influenza virus,56,60,61,64,65 West Nile virus,126

St. Louis encephalitis virus3,50,51 and Western Equine En-cephalitis virus49 and fungi like Cryptococcus spp..43,44,46

These have been isolated from many wild birds using stan-dard serological3,30,47,48,50,51,56,60,61,64,65,79 and microbio-logical techniques.28,31e33,37,43,44,46,79,126,127 Moreovervectors with the ability to carry pathogens have also beenisolated from wild birds.3,37,85,87 For example, ornithophilicmosquitoes and ticks are the principal vectors of pathogenslike West Nile virus in the Old World, and B. burgdorferi, re-spectively, and birds of several species, chiefly migrants,appear to be the major introductory or amplifying hostsof these vectors.3,37,85,87

Methods that have been used to confirm association ofmicrobial agents isolated from wild birds with infection inhumans include molecular methods like sequence analysisfor Ehrlichia85 and Mycobacterium species,32,33 phyloge-netic analysis,25 pulsed-field gel electrophoresis,26 poly-merase chain reaction,26 immunomagnetic separation(IMS) for E. coli,25,26 serological methods for influenzavirus56,59 and psittacosis,17 and epidemiological methodsfor Salmonella spp.,28,29 Borrelia spp.,36 West Nile vi-rus,30,48,49,126 St. Louis encephalitis virus,49,51 and WesternEquine Encephalitis virus.49

However, in most scientific literature, there is no de-tailed data regarding the detection and characterization ofpathogens and their relation to wild birds. In most of thecases, it seems that wild birds serve as vectors of thepathogen. In these cases, the indirect role of wild birds intransmission of the infectious agents can be only specu-lated and the implicated pathogens are classified as having

the theoretical risk of transmission from wild birds tohumans (Table 2).

Twenty-one wild avian family species were identifiedthat are reservoirs, mechanical vectors or both for in-fectious agents that may affect humans (Listed with theirformal family names in the appendix according to the Sibleyand Monroe Classification for birds). A short description ofpathogens that may be transmitted from wild birds tohumans is outlined below.

Types of microorganisms carried by wild birds thatcould affect humans (indirect transmission ortheoretical risk)

BacteriaA range of bacterial pathogens affecting humans has beenassociated with wild and migratory birds. An indirecttransmission to humans has been reported for some ofthese such as the enteric pathogens E. coli24 and Salmo-nella spp.28,29 Tick-borne pathogens such as Borrelia burg-dorferi sensu lato species have been also associated withhuman infection from wild migratory birds.35e38,85,87 A the-oretical risk for transmission to humans has been reportedfor other bacterial pathogens such as Yersinia spp.,76,128

Campylobacter jejuni77 and both cholera and non-choleraVibrio spp.92

FungiYeasts and yeast-like fungi have been isolated from wildand migratory birds such as Candida spp.,129,130 and hypho-mycetes e.g. Aspergillus spp., Microsporum spp., Tricho-phyton spp.,112 and cryptococci.43 A theoretical risk fortransmission to humans exists but scientific data to supportthis are extremely scarce. Cryptococci that are quite ubiq-uitous in nature have been reported to be transmitted tohumans indirectly from wild pigeons (Columbidae), occa-sionally causing clinical infection, especially in immuno-compromised patients.42

VirusesImportant viral species have been isolated from wildmigratory birds and can affect humans indirectly includinginfluenza A viruses,62,131 the West Nile virus (WNV),3,47 theSt. Louis encephalitis virus (SLEV).3,50,51 Several other viralspecies can theoretically be transmitted from wild birds tohumans (Table 2).

ParasitesWild and migratory birds can disperse in nature a diversenumber of protozoa such as Babesia and other haemopara-sites. The potential for transmission exists for some para-sitic species (Table 2).

Factors potentially contributing in transmission

The issue of the transmissibility of various pathogens fromwild birds including migratory species to humans is fairlycomplex. Several factors determine the possibility of sucha spread. Some factors relate to the affected speciesincluding the birds themselves (e.g. the avian speciesinvolved, susceptible local vertebrate recipients or

Table 2 Pathogens with theoretical risk for transmission (but no reports of actual direct/indirect transmission) from wild birds including migratory species to humans

Microorganism(s) Potential for transmission to humans exists (n Z 50) Migratory bird species Geographic area

(I) BacteriaGram-positive cocciEnterococcus Possible spread through polluted water67,68;

transmission has been reported from other birds69e71Ducks (Anatidae), seagulls (Larus), waterfowls(Anatidae) and other migratory birds such as quails(Coturnix)

Worldwide

Staphylococcus Possible through faecal pollution of environmentalwater samples72

Ducks (Anatidae), mallards (Anas platyrhynchos),passerines (Passeriformes), seagulls (Larus), andother migratory birds including quails (Coturnix),raptors (North American raptors)

Worldwide

Gram-positive rodsClostridium perfringens Possible through accidental ingestion of

contaminated water73; food-borne enteritis has beenreported from non-migratory birds74

Crows (Corvidae), ducks (Anatidae), gulls(Larus),Pelicans (Pelecanus) and marine birds, raptors (NorthAmerican raptors), shorebirds (North Americanshorebirds), waterfowls (Anatidae)

Europe, Asia

Listeria monocytogenes Possible through accidental ingestion ofcontaminated water75

Crows (corvus), gulls (Larus), rooks (Corvusfrugilegus) and other migratory birds

America, Asia

Enterobacteriaceae Enteritis30,76 Crows (corvus), ducks (Anatidae), gulls (Larus),magpies, (Corvidae) pigeons (Columbidae),pheasants, starlings (Sturnidae), terns (Sternidae),wagtails (Motacilla), waterfowls (Anatidae) and othermigratory species

WorldwideYersinia species

CampylobacteraceaeCampylobacter jejuni Intestinal campylobacteriosis.30,77,78 Whether

waterfowl (Anatidae) have a role in the disseminationof Campylobacter spp. that results in increasedhuman disease is likely to be elucidated throughdevelopment and greater use of typing methods.79

Typing might allow links to be established betweenisolates of avian, environmental, and human origin.79

Migrating ducks (Anatidae), passerine birds e.g.crows (corvus), pigeons (Columbidae) and seagulls(Larus), sparrows (Passeridae)

Europe, North America,Asia

Helicobacter spp. Enteritis (Helicobacter canadensis).80,81 Geese (Anserinae), gulls (Larus), passerines(Passeriformes), terns (Sternidae), various wild birds

North America, Europe,AustraliaPossible transmission of H. pylori by contaminated

water from feces of waterfowls (Anatidae)82

Other gram negativebacilli (Pseudomonas,Aeromonas, etc.)

Possible through faecal pollution of environmentalwater samples72,83

Geese (Anserinae), gulls (Larus) Worldwide

Anaerobic bacteria Possible through faecal pollution of environmentalwater samples e.g. gulls (Larus)84

Geese (Anserinae), seagulls (Larus), swans(Cygninae), wild ducks (Anatidae)

Worldwide

Anaplasmataceae Human granulocytic ehrlichiosis85e87 Passerine birds (Passeriformes) American Robins(Turdus migratorius), robins, songbirds(Passeriformes) veery (Catharus fuscescens),American warbler

North America, Europe,AsiaAnaplasma

phagocytophilum

88S.

Tsio

dra

set

al.

Mycobacterium species Tuberculosis.88 Possible transmission ofmycobacterium from humans to birds has beenreported through close contact between humans andpet birds but it is not known if humans can acquirethe infection from birds.88

Green-winged macaw, psittacines(Psittaciformes)88,89M. tuberculosis

Rickettsiaceae Possible through ticks 90,91 Pigeons (Columbidae) Europe, AsiaCoxiella burnetii

VibrionaceaeVibrio cholerae Cholera, non-cholera Vibrio infections92,93 Wild aquatic birds (Anatidae), gulls (Larus) North America

(II) VirusesBunyaviridae Possible transmission through ticks and transmission

has been reported for other birds94,95Crows (Corvidae), wild aquatic birds (Anatidae),passerines (Passeriformes), rooks, (Corvus frugilegus)

Europe, Asia, AfricaNairoviruses: Crimean-

Congo haemorrhagicfever (CCHF)

Coronaviridae Serological evidence in humans exposed to birds hasbeen reported96

Passerines (Passeriformes), pheasants (Phasianidae) WorldwideAvian infectious

bronchitis virus, othercoronaviruses

Flaviviridae WorldwideJapanese encephalitis

virus (JEV)Yes97e99 Colonial ardeids (Ardeidae), herons (Ardeidae),

marsh birds, quails (Coturnix)Other flaviviruses

Murray Valleyencephalitis virus(MVEV), Usutu virus(USUV)

Yes (MVEV)100,101 Blackbirds (Turdus merula), wading birds, crows andmagpies (Corvidae) (Usutu virus), Pelecaniformes(MVE virus)

NR (USUV)

Sindbis virus Ockelbo disease,102,103 Pogosta disease,104 pluspossible transmission to humans as migratory birdsare hosts of mosquitoes which are vectors for theseviruses

Blackbird (Turdus merula), carrion crow (Corvuscorone), passerine birds (Passeriformes) wild grouse(Tetraonidae), wild ducks (Anatidae)

Tick-borne Encephalitisvirus (TBE)

Possible through ticks 105e108 Blackbirds (Turdus merula), sandpipers(Scolopacidae), wild mallards (Anas platyrhynchos),wild grouse (Tetraonidae), other wild birds

Europe, America

Herpesviridae Marek’s virus (transported by wild birds) has beenassociated with multiple sclerosis in humans.109,110

Japanese quails (Coturnix coturnic japonica),passerines (Passeriformes), pigeons (Columbidae),raptors (North American raptors), wild anseriforms(Anatidae), geese (Anserinae), swans (Cygninae)

Europe, Asia, NorthAmerica, and AfricaAnatid herpesvirus 1,

(duck plague virus),Marek virus

ParamyxoviridaeNewcastle disease virus

(NDV, avianparainfluenza virus 1,paramyxovirus-1)

Serological evidence in humans exposed to migratorybirds has been reported.96 Can cause self-limitingconjunctivitis as occupational exposure to affectedpoultry

Cormorants (Phalacrocoracidae), gulls (Larus),passerines (Passeriformes), pelicans (Pelecanus),raptors (North American raptors), waterfowls(Anatidae)

Worldwide

(continued on next page)

Wild

bird

sand

hum

an

infe

ctions

89

Table 2 (continued)

Microorganism(s) Potential for transmission to humans exists (n Z 50) Migratory bird species Geographic area

Other Paramyxoviridae(pneumoviruses)

NR Gulls (Larus), waterfowl (Anatidae) Europe, Africa, Asia

PicornaviridaeEgg drop syndrome virus Possible through faecal pollution of environmental

water samples with wildfowl droppings111,112Coots (Fulica), grebes (Podicipedidae), herring gulls(Larus argentatus), migratory ducks (Anatidae), owls(Strigidae), storks (Ciconiidae), swans (Cygninae)

Worldwide

Foot-and-mouth diseasevirus

NR but according to some studies birds do not have animportant role in the transmission of enteroviruses113

House-sparrows (Passer domesticus), seagulls(Laridae), starlings (Sturnidae)

Europe

Reoviridae Not reported but evidence for transmission tomammals111,114e116

Wild geese (Anserinae), wild woodcocks (Scolopax) Asia, Africa, Europe,AmericaAvian rotavirus, orbivirus

and other spp.

TogaviridaeEastern (EEE ) and

Western (WEE ) equineencephalitis viruses

Possible through mosquitoes that are vectors forthese viruses117,118

Cliff swallows (Petrochelidon pyrrhonota), finches(Fringillidae), American Robins (Turdus migratorius,smaller species of Passeriformes, several trans-Gulfmigrant starlings (Sturnidae), waterbirds (Anatidae)

America

Venezuelan equineencephalitis virus(VEE)

Possible through mosquitoes that are vectors forthese viruses 119,120

Nestling birds such as Cliff swallows, North Americanshorebirds, songbirds (Passeriformes), wild ducks(Anatidae)

South to Central America

(III) ParasitesCoccidia (Eimeria) Possible through contamination with faecal

material121Cranes (Gruidae), owls (Strigidae), wild pigeons(Columbidae), waterfowls (Anatidae)

North America,Asia, Africa

Cryptosporidium Has been reported for other non-migratory birds122 Cranes (Gruidae), exotic seagulls (Larus), wildanseriforms: ducks (Anatidae), geese (Anserinae),swans (Cygninae) and wild birds (orderPasseriformes, Phasianidae, Fringillidae, andIcteridae), waterfowl species (Anatidae)

America, Africa, Asia

Helminths parasites Possible food-borne through eating small waterfish.123

Gulls (Larus), ducks (Anatidae), passerines(Passeriformes), waterfowl species (Anatidae)

Australia, Europe,Africa, Asia, America

Cercarial dermatitis (swimmer’s itch) due toexposure to marine schistosomes124

Sarcocystis Possible through contaminated water125 Cowbirds (Molothrus), exotic birds, mallards (Anasplatyrhynchos), passerines (Passeriformes), wadingbirds, wild anseriforms (Anatidae), geese(Anserinae), swans (Cygninae)

America, Africa, Europe

90S.

Tsio

dra

set

al.


invertebrate vectors), others to the pathogen itself (e.g.stability of the agent in the environment), and lastly somefactors relate to the environment (e.g. temperature,humidity). Studies of certain pathogens like influenza virusillustrate the interaction of factors that limit the trans-mission and subsequent establishment of an infection ina novel host species and may help us in understanding howand why some pathogens become capable of crossing hostspecies barriers.132

Factors relating to the implicated pathogen and theaffected speciesPathogens associated with wild and migratory birds may betransmitted to humans via several routes. Generation ofcontaminated aerosols by waterfowl flocks may result inrespiratory infections through inhalation of dust or finewater droplets generated from infected bird feces orrespiratory secretions in the environment (e.g. NewcastleDisease or chlamydiosis).30 Birds can contaminate waterwith feces, nasal discharges, and respiratory secretions(e.g. influenza A virus, Enterobacteriaceae) resulting ina waterborne human infection after direct contact withaquatic environments.30 Recently, the European CDC con-cluded that the bathing risk in the case of waters contam-inated with the H5N1 virus cannot be excluded and shouldbe assessed on a case by case basis even though the chanceof such an event is highly unlikely.133 Food-borne infectionsmay result after consumption of infected carcasses of wildbirds or raw or undercooked blood, organs, or meat, e.g.,WNV, avian influenza A (H5N1), M. avium, Clostridiumspp., Sarcocystis, Frenkelia.52,63,134 Infections may lastlyresult after direct contact with the skin, feathers, externallesions or droppings of infected wild birds (e.g. avian pox,WNV encephalitis, H5N1, mycoplasmal conjunctivitis). Amajor source of wild birdehuman contact is hunting andthe cleaning of killed birds. Often birds are field-dressedby hunters with minimal protection bringing them in con-tact with blood, organs and feces.30 Serologic evidence ofavian influenza infection in hunters and wildlife profes-sionals has been reported.56 In addition, occupational expo-sure to avian species (e.g veterinarians) may increase riskof infections like avian influenza virus infection. Indirectinfection may occur through the same routes if wild birdstransmit the infection to domestic animals, e.g. poultryor via exposure to inanimate surfaces contaminated bybird secretions or droppings. Transfer of infected materialcan happen with shoes, clothing or other inanimate objects.

Wild birds when serving as reservoirs exhibit multiplica-tion of the pathogen within their organism. Aggregations ofbird species that occur during certain periods within theavian annual cycle may enable transmission of pathogensbetween individuals. Extreme examples for such aggrega-tions can be found at moulting and staging areas of earedgrebes Podiceps nigricollis,135,136 at roosting sites for Euro-pean starlings Sturnus vulgaris, at landbridges betweencontinents (e.g. Gibraltar, Bosporus) widely used by soaringand gliding species like larger birds of prey and white storksCiconia ciconia and at breeding sites of many seabirds. Interms of numbers, the vast amount of migratory birds domigrate solitarily in ‘broad front’ and therefore do not en-counter an increased risk of pathogen transmission, while

some species travel hundreds to thousands of kilometresfrom their breeding grounds and re-fuel at distinct stopoversites.137 These ‘‘staging areas’’ provide the opportunity forclose intermingling of species that are otherwise widelyseparated during the major part of the year.35,138 Thus,the theoretical opportunity for exchange of pathogens is in-creased among avian species, which make use of the samestopover sites. In such instances duration and concentrationof the agent in the blood or the gastrointestinal tract of mi-grating birds are important for the subsequent infection ofanother competent vector that feeds or gets exposed incrowding situations or during stopover e.g. a tick. Severalstudies have recorded infections e.g. B. burgdorferi andhuman granulocytic ehrlichiosis (HGE) in ticks removedfrom birds.36,37,87 Ticks commonly infest a wide range ofavian species, especially, sparrows (Passeridae), thrushesand other ground foraging birds.30,36,37,139,140 Althougha wide range of tick species has been reported to parasitizewild birds, Ixodes spp. are the most likely ones to carry in-fections (e.g. B. burgdorferi) especially in Europe andNorth America. Ixodid ticks often attach to hosts for 24e48 hours while acquiring a blood meal. In tick-borne vi-ruses, bacteria, and protozoa, the infectious larval ornymphal tick may remain attached to the body of a migra-tory bird for several days and then deposited during migra-tion in a new geographic area. During migration, there issufficient time for some birds to travel hundreds or evena few thousand miles before ticks complete feeding anddrop off. Even if these birds have small tick burdens, theirlarge numbers could result in substantial contributions tolocal tick populations in coastal areas.40 There is even evi-dence of transhemispheric exchange of spirochete-infectedticks by seabirds indicating the capacity for wild birds tocarry infected ticks for long distances.141 Moreover, birdscan carry infections in their bloodstream which is intro-duced to local population of ticks at other sites. Therefore,birds play an important role not only in maintaining infectionssuch as B. burgdorferi sensu lato in areas of endemicity, in ad-dition some of them, through their migration, also play a roleby spreading ticks within and between continents.36,139,142,143

Exposure to tick-borne diseases is primarily peridomestic,so the contribution to tick related human infection of avianticks relative to mammalian ticks around dwellings is criti-cal.38 Birds that are implicated in peridomestic transmissionof tick related infections to humans, especially in NorthAmerica, include American robins (Turdus migratorius),northern cardinals (Cardinalis cardinalis), and song sparrows(Melospiza melodia) that frequently use backyard environ-ments and some of which are commonly seen at bird feeders.Therefore, they are likely to drop engorged larvae in perido-mestic environments like lawns and gardens,40 where ticksare less common than in woods and at wood edges butmore likely to encounter people.38,144 Even though the sur-vival of nymphs is low in open habitats, the contribution ofbirds to human infection in the peridomestic environmentcould be substantial and deserves further study.40

An additional factor is the physiologic stress that wildmigratory birds suffer with migration, a risk factor forimmunosuppression and increased susceptibility to infec-tious diseases. Avian species may exhibit an increasedsusceptibility to certain pathogens (e.g. West Nile virus)compared to other vertebrate groups.3,4 Changes and


adaptations occur in migratory birds during long-distancemigration.63 For some birds, the stress of migration canlead to reactivation of otherwise latent infections.145

West Nile virus was isolated from migrating birds thatwere under migratory stress.146 However, an opposingargument is that infected migratory birds could not survivelong-distance travel; thus their role in transmitting commu-nicable diseases is of less importance.147 For example, inthe case of avian influenza most outbreaks in wild birdsseem to reflect local acquisition of infection from a contam-inated source, followed by rapid death nearby.148 There isonly limited evidence that some wild birds can carry the virusasymptomatically, and no evidence from wild bird outbreaksthat they have done so over long distances during seasonalmigration.148

Understanding the balance between the changes andadaptations that occur in migratory birds during long-distance migration is important to comprehend susceptibil-ity of certain migratory birds to develop infections. Similarfactors e.g. age and bird gender may in addition influencemigratory patterns leading to spread of diseases in novelgeographical areas.3

Factors relating to the implicated pathogen and theenvironmentMigrants of most bird species in the New World seldom usethe same stopover sites on northward, spring migration asthey do on southward, fall migration. This is becausemigration routes are determined by complex interactionsof environmental factors such as direction of prevailingwinds, weather patterns, location of available food re-sources and geographical barriers (e.g. large bodies ofwater, deserts and mountains). These factors seldomcombine to favour the same route in different seasons.3

Seasonality is a significant factor influencing both, wildbirds (wild resident and migratory species) and other vec-tors e.g. mosquitoes, ticks leading to changes in transmis-sion dynamics.149e151 For mosquitoes, a spring populationpeak in Europe and North America occurs during the springmigration of birds.146e148 The effect of seasonality in theflyway patterns of major migratory birds was observed forcertain diseases such as West Nile virus encephalitis. Theincidence of West Nile virus disease is seasonal in the tem-perate zones of North America, Europe, and the Mediterra-nean Basin, with peak activity from July throughOctober.152 Both avian and human infection rates drop tonear zero as winter approaches and mosquitoes becomedormant.153 Season is important for some non-vector-bornepathogens, as well. For example, influenza A viruses remaininfectious in water at lower ambient temperatures and atthe same time major congregations of migratory waterfowloccur, increasing the likelihood of transmission amongbirds. Furthermore, numerous bird species (e.g. crowsand gulls) are attracted to untreated sewage, garbagedumps, manure, and other sources of enteric pathogensthat can then be transmitted to humans. These areasshould be appropriately covered and not open to the accessof wild migratory birds.

Migratory bird flyways and transmissionLong-distance migration is one of the most demandingactivities in the animal world and several studies demonstrate

that such prolonged, intense exercise leads to immunosup-pression exacerbating the possibility of spreading infec-tions. On the other hand, infected symptomatic wild birdsmay act as vectors over shorter distances.154 Understandingbird migration, avian migration patterns and infectious dis-eases of birds would be useful in helping to predict futureoutbreaks of infections due to emerging zoonotic pathogensand can provide important information that could explainthe pattern of spread of certain infectious agents. Numer-ous variations in flyways exist. For some ocean migratorywild birds, a nomadic wandering that can appear randomis probably related to poorly understood weather or oceanconditions.155,156 Major migratory flyways, especially be-tween continents are known to be used by migratory birdswhen commuting between breeding and wintering areasand vice versa. Nevertheless, these flyways are only usedby a fraction of the existing species on the move, predom-inately by waterfowl and soaring and gliding migrants likelarge raptors and storks which aggregate and follow fairlyeasily defined routes.

The complex overlapping of major flyways and the lackof information on migratory species potentially involved inthe spread of disease make simple association of wildmigratory flyways with outbreaks of certain infectionsextremely difficult despite the significant amount of liter-ature on the subject. For example, in Alaska, there isa notable overlap between the Pacific and East Asia/Australasia flyways through which scientists believe avian-flu-infected migrating birds, such as the bar-tailed godwit(Limosa lapponica), dunlin (Calidris alpina), and red knot(Calidris canutus), will transfer the Asian strains of H5N1 in-fluenza virus to North American birds over the next fewmonths14 although this was not confirmed in a recentstudy.157 On the other hand, other more local migratorybird routes have been described in association with WestNile virus outbreaks.3

Societal factorsFurthermore, societal factors like captivation of wild birdsin zoos and importation and sale of wild birds as pets shouldalso be considered as important factors which can enhancethe spread of pathogens from wild birds to humans. Crypto-sporidium has been reported to be transmitted from somenon-migratory birds in zoos to humans.122 A theoretical sim-ilar risk for avian influenza exists as avian influenza was re-cently isolated from a wild swan in the Dresden zoo inGermany.157 Similar risk can be encountered in bird parkssince outbreaks of infections related to birds like psittaco-sis have occurred.17 Finally, the international trade ofexotic pet birds carrying influenza A viruses enhances therisk of worldwide dissemination of potentially virulent influ-enza A virus and may pose a serious health threat tohumans.158

Limitations of the current literature review

There are several limitations of this work and clearlyfurther work is necessary. Some of the identified agentsare quite ubiquitous in the environment raising the questionabout how to quantify the additional impact wild resident


and migratory birds may have on transmission. There is stillscientific debate over the actual role migratory birds mightplay in the transmission of certain communicable diseases.In support of this argument we did not find any evidence fordirect transmission from wild and migratory birds tohumans for any of the identified pathogens the onlyexception being the cluster of H5N1 human cases inAzerbaijan.16 In addition, in many cases, there was no fur-ther available information that would allow further elucida-tion of the real epidemiological role played by wild birds inthe ecology of the considered infections, especially in un-derdeveloped countries. Many reports do not exactly clarifyhow the birds are implicated in the transmission of these in-fections and in the majority of cases this transmission couldnot be established by adequate scientific methods. Thus, inmany of the reports reviewed herein, there were no dataregarding serologic assays or molecular diagnostic tech-niques used to detect and characterize pathogens and iden-tify birds as vectors of disease. In these cases onlyassociations of these infections with migratory birds couldbe made (Table 2).

The evidence reviewed herein suggests that manypathogens can infect multiple host bird species and thatthese pathogens in theory could be responsible for emerg-ing infectious disease outbreaks in humans and wildlife.However, the ecologic and evolutionary factors that con-strain or facilitate such emergences are poorly understood.In the literature, a different terminology is used to describethe interaction between hosts, including wild birds, andpathogens. Terms such as multihost pathogens, reservoirhosts, and spill-overs are frequently used, but often suchdifferent terms are used to describe the same phenome-non. There is a need for a single, standardised comprehen-sive framework that characterizes disease outcomes basedon biologically meaningful processes. An example of suchconceptual framework is based on the pathogen’s between-and within-species transmission rates and can be used todescribe possible configurations of a multihostepathogencommunity.159 In particular, the much-overused terms res-ervoir and spill-over can be seen to have explicit defi-nitions, depending on whether the pathogen can besustained within the target host population.159 However,the paucity of available published data did not allow usto determine whether the involved species of certain wildbirds serve as reservoir or spill-over. Finally, only few stud-ies have reviewed the role of migratory birds in transmis-sion of all different infections and these studies remaindescriptive.112

Migratory birds cannot be blamed for recurrent out-breaks at the same geographical location over subsequentyears unless there is in an introduction of the pathogen toknown or novel avian or other animal reservoir hosts andvectors. Furthermore, for some viruses that are consideredto be transmitted by wild migratory birds (e.g. West Nile vi-rus), duration of high levels of viremia for most speciestested has been found to be limited and usually less than24 hours. However, exceptions to that rule exist. The housesparrow (Passer domesticus) has demonstrated WNV vire-mia of sufficient duration to indicate its ability to serveas a competent host for WNV.3

Furthermore, other modes of transmission such as theimport of infected products may be of equal importance in

the spread of diseases like avian influenza and scientistsare still debating the evidence of the role of migratory birdsin the wide geographical spread of the influenza A (H5N1)virus. Highly pathogenic avian influenza viruses have beenisolated rarely from wild birds and, apart from a singlecase in common terns in South Africa,160 when they have,it has usually been in the vicinity of outbreaks of highlypathogenic avian influenza virus in poultry or geographi-cally and chronologically close to known outbreaks in poul-try. In fact the de novo generation of highly pathogenicavian influenza virus strains (restricted to subtypes H5and H7) so far has been described to have occurred onlyin domestic poultry and the occurrence of highly patho-genic avian Influenza viruses in wild birds is most likelythe result from spill-overs from the poultry population.

Another important limitation is that there is no way topredict whether the comprehensive lists presented in thispaper may expand in the near future. Moreover, the factthat a lot of the pathogens carried by wild and migratorybirds that are presented in Table 2 have not been associ-ated with human infection does not mean that these path-ogens cannot cause human infection through routespresented for other pathogens in the same table.

Future directions

Identifying links between environmental factors and in-fectious disease risk is essential to understanding howhuman-induced environmental changes will affect thedynamics of human and wildlife diseases. Studying largewetland areas, and by extension, intact wetland birdcommunities, may represent a valuable ecosystem-basedapproach for controlling infections caused by migratorybirds including WNV.161 Recent evaluations suggesting linksbetween high biodiversity among wild birds and reducedvector-borne disease risk, such as WNV, may lead to a betterunderstanding of distribution patterns of such diseases.48

Recent findings on the origin of the WNV infections suggesta single species to act as a super spreader and the transmis-sion of WNV appears in new light.162 These recent findingsdemonstrate imposingly how important detailed studieson contact rates between vectors and host species areand how careful interpretations need to be made beforedrawing any conclusions. Estimation of the infection rateof wild bird populations with human pathogens or withother vectors carrying pathogens is clearly an indicated fu-ture challenge required to judge the possibilities of bird tohuman transmission of pathogens. The same accounts forthe transmission between and within bird species. Recentinvestigations indicate the influence of social and sexualbehaviours and their seasonal components on intra-specifictransmission,163,164 while the inter-specific transmissionrate remains speculative. Birds are considered to show be-havioural changes due to pathogen infection, which willconsiderably influence transmission rates.163 Furthermore,accurate data on the speed and direction of migratory birdsmay enable us to predict the timing of bird migration inmore detail; this will assist in monitoring the risk of infec-tions that may be caused by wild birds. While this knowl-edge is available for larger bird species due to the use ofsatellite tracking, only limited data are available on the

Supplementary data

Supplementary data associated with this article can befound, in the online version, at doi:10.1016/j.jinf.2007.11.001.


individual level for some North American songbirds with theuse of radio-telemetry tracking.165 Producing maps depict-ing the ecology of the vectors including mosquitoes andticks ecology in combination with maps of migratory routesof wild birds along with access to real time climatic datacould be the key for developing a real time early warningsystem for forecasting vector-borne disease outbreaks.166

The spatial and temporal pattern of migration of wildbirds as well the spatial distribution throughout the annualcycle can provide further insight. Application of stableisotope analysis has already resulted in new insights wherebird populations spend the time between the seasonallyreoccurring breeding events,167 a knowledge which can beof great importance for future predictability of diseaseoutbreaks.

Human medicine often does not delve deeply into therole of animals in the transmission of zoonotic agents andveterinary medicine does not cover the clinical aspects ofhuman disease. However, to effectively and completelycover the area of infections associated with wild birdswould require involvement of both physicians and veteri-narians especially those dealing with avian species.168

Unfortunately, one recent study demonstrated that com-munication between physicians and veterinarians aboutzoonotic diseases is largely absent.168 Therefore, one im-portant factor that could potentially explain the paucityof available data regarding the transmission of pathogensfrom wild birds to humans could be the lack of communica-tion between physicians and ornithologists. To most effec-tively decrease the risk of infections associated with wildbirds, the public health and animal health sectors must col-laborate in developing strategies to decrease human expo-sure to pathogens carried by wild birds.

An effective public educational campaign could also putin perspective and clarify myths and realities about the riskof acquiring infections associated with wild birds. Activitiesnear geographical areas with extensive wild bird activityreally carry minimal risk especially if people take personalprotective measures for high risk activities such as handlingdead wild waterfowl. Normal behaviour that complies withgeneral hygienic standards should suffice.

Conclusions

We attempted to summarize the published scientific evi-dence regarding the direct and indirect roles of wild birds intransmission of certain infections to humans. Although wecould not fully define this role and it appears that furtherresearch is necessary, several conclusions can be made.First, there is no real evidence for direct wild birdehumantransmission besides rare examples occurring under excep-tional circumstances. Several human infections can theo-retically be transmitted from wild and migratory birdsalthough the scientific base for most of the associationsremains speculative. These findings are expected forzoonoses, which usually require the amplification in ananimal species cycle before spill-over to humans. Wild andmigrant birds are most important in seeding pathogens intothese amplification systems. This explains why most of theassociation with transmission from bird to human mayonly occur indirectly. On the other hand, there is strong

evidence for the dispersal of pathogens to new geograph-ical locations by migrating birds but it is largely unknownhow this will affect transmission to humans. The recentemergence of infections like West Nile virus and influenzaA in various parts of the world is a prominent example ofhow rapidly and widely a migratory bird associated diseasecan spread. The potential factors and mechanisms involvedin the transmission of such infectious agents from birds tohumans need further elucidation. An in-depth comprehen-sion of avian migration routes as well as further researchusing advanced molecular testing of the prevalence, patho-genesis, and clinical associations of several pathogens thatare transmitted to humans from the various migratory birdspecies would lead to a better understanding of the transmis-sion dynamics of diseases carried by avian species helping topredict future outbreaks of relevant human infections.

Conflict of interest

None.

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